AbstractPlant respiration is an important contributor to the proposed positive global carbon‐cycle feedback to climate change. However, as a major component, leaf mitochondrial (‘dark’) respiration (Rd) differs among species adapted to contrasting environments and is known to acclimate to sustained changes in temperature. No accepted theory explains these phenomena or predicts its magnitude. Here we propose that the acclimation of Rd follows an optimal behaviour related to the need to maintain long‐term average photosynthetic capacity (Vcmax) so that available environmental resources can be most efficiently used for photosynthesis. To test this hypothesis, we extend photosynthetic co‐ordination theory to predict the acclimation of Rd to growth temperature via a link to Vcmax, and compare predictions to a global set of measurements from 112 sites spanning all terrestrial biomes. This extended co‐ordination theory predicts that field‐measured Rd and Vcmax accessed at growth temperature (Rd,tg and Vcmax,tg) should increase by 3.7% and 5.5% per degree increase in growth temperature. These acclimated responses to growth temperature are less steep than the corresponding instantaneous responses, which increase 8.1% and 9.9% per degree of measurement temperature for Rd and Vcmax respectively. Data‐fitted responses proof indistinguishable from the values predicted by our theory, and smaller than the instantaneous responses. Theory and data are also shown to agree that the basal rates of both Rd and Vcmax assessed at 25°C (Rd,25 and Vcmax,25) decline by ~4.4% per degree increase in growth temperature. These results provide a parsimonious general theory for Rd acclimation to temperature that is simpler—and potentially more reliable—than the plant functional type‐based leaf respiration schemes currently employed in most ecosystem and land‐surface models.